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Manzini, M. C.

Publications and source records attributed to Manzini, M. C..

8 recordsLinked to original sources

Removal of maternal compensation reveals retinal-specific roles for Pomgnt1 in zebrafish

Genetic variants in Protein O-mannose N-acetylglucosaminyltransferase 1 (POMGNT1) result in a broad spectrum of disorders, ranging from severe congenital muscular dystrophy with brain and ocular malformations to non-syndromic retinitis pigmentosa. Despite POMGNT1's established role in the glycosylation of the transmembrane glycoprotein &alpha-dystroglycan (&alpha-DG), the mechanistic basis for this clinical variability remains poorly understood. Previous work in a zebrafish pomngt1 knock-out (KO) line identified retinal degeneration at 6 months post-fertilization (mpf). However, potential involvement of other tissues was not characterized, and compensation from maternal transcripts which can occur in the zebrafish oocyte was not tested. Here, we analyzed maternal-zygotic pomgnt1 KOs (MZKOs) to determine whether maternal compensation influences the onset and severity of pomgnt1-associated phenotypes. We assessed survival, gross morphology, locomotor activity, behavioral patterns, and retinal organization across multiple timepoints. MZKOs survived to adulthood and exhibited no morphological or locomotor deficits up to 5 mpf. Retinal abnormalities were found as early as 2 mpf in MZKOs, demonstrating that maternally provided factors of pomgnt1 delay the onset of retinal pathology. Additionally, MZKOs displayed a novel wall-hugging behavioral pattern that may be consistent with visual impairment or anxiety. These findings demonstrate a strong tissue-specific phenotype following loss of pomgnt1 in zebrafish showing evolutionary divergence in the necessity for Pomgnt1 function in the muscle. However, this strain provides a useful system for investigating the mechanisms underlying the retinal vulnerability observed in POMGNT1-related retinitis pigmentosa.

genetics↗

Dose dependent impact of global Cc2d1a reduction on cognitive, social, and metabolic phenotypes

Background Autism spectrum disorder (ASD) and Intellectual disability (ID) share an in-creased male prevalence, but the biological mechanisms underlying this male bias remain poorly understood. Mice deficient for CC2D1A, a protein scaffold mutated in ASD/ID, have shown multiple male-specific deficits both in ASD-like behaviors and in the regulation of neuronal intracellular signaling pathways. However, previous re-search relied on conditional knockout (cKO) models due to early postnatal lethality of global Cc2d1a KO strains. Thus, the ability to define the developmental impacts of CC2D1A LOF in mice has been limited. While generating a Cc2d1a knock-in strain with V5-HA epitope tags, we found that homozygous animals (Cc2d1aVH/VH) resulted in a hypomorph line that can be used to study developmental loss of CC2D1A. Methods We assessed gross morphology, behavior, and intracellular signaling in male and female Cc2d1aVH/VH animals, where only ~20% of CC2D1A is present. We then crossed this line with a null allele to obtain a more severe hypomorph (Cc2d1a-/VH) and explore phenotypic penetrance thresholds. In addition to the previous phenotypic characterization, we also assessed body composition, feeding, and molecular hall-marks of metabolic function in both sexes. Results We found that ~80% CC2D1A reduction in Cc2d1aVH/VH mice did not recapitu-late any of the behavioral or molecular disruptions seen in cKO models. In contrast, ~90% CC2D1A reduction in Cc2d1a-/VH mice resulted in ASD/ID-like behavioral phe-notypes in males, similar to those reported in cKO lines, with distinct intracellular sig-naling disruptions. Male and female Cc2d1a-/VH mice also showed subtle but signifi-cant adult weight deficits associated with distinct metabolic changes. Limitations These models still do not fully recapitulate the complete CC2D1A LOF found in patients. Due to the analysis of two independent strains over multiple metrics, these studies are not powered to compare statistical differences between sexes and data were analyzed in males and females independently. Conclusions We identified a strikingly narrow CC2D1A expression threshold for the emer-gence of ASD/ID-like behavioral deficits in males. In addition, we revealed a novel role for CC2D1A in adult weight gain. These mouse strains will be useful to better under-stand CC2D1A LOF phenotypes.

neuroscience↗

Interactome Analysis of the CC2D1A Scaffold Reveals Novel Neuronal Interactions and a Postsynaptic Role

Loss of the protein scaffold Coiled-coil and C2 domain containing 1A (CC2D1A) leads to intellectual disability (ID), autism spectrum disorder (ASD), and other neurodevelopmental presentations in humans. CC2D1A interactions have been studied in different cell lines proposing diverse roles in endolysosomal maturation and intracellular signaling, but the composition and functional mechanisms of the CC2D1A interactome remain poorly understood, especially in the brain. We performed comprehensive proteomic analyses to characterize CC2D1A binding partners, first comparing immunoprecipitations with three different anti-CC2D1A antibodies in HEK293 cells and then probing the mouse hippocampus. In HEK cells, Gene Ontology (GO) analysis revealed broad interaction networks in the nucleus, mitochondrion, and cytoplasmic vesicles sharing functions in organelle organization, vesicle mediated transport, and protein metabolism. These are unified by the best characterized CC2D1A interactor, the ESCRT III component CHMP4B, and define a pleiotropic role for CC2D1A in membrane trafficking and protein homeostasis. In the hippocampus, using stringent criteria and additional controls, including a Cc2d1a hypomorph mouse line, we identified 10 high-confidence interactors in addition to CHMP4B (TNIK, G3BP2, CEP135, MAPKAP1, SHFL, PPT1, PNKD, VAMP5, and PPP6R2) revealing roles for RNA regulation and synaptic function. The HEK studies had also pointed to CC2D1B, the only paralog of CC2D1A, as an interactor. We confirmed that not only the two proteins can bind in the brain, but also localize in different synaptic compartments, showing that CC2D1A is uniquely enriched in the post-synapse. This supports a unique function of CC2D1A in regulation of synaptic transmission that could explain the more severe cognitive deficits in humans and mice upon its loss. To our knowledge these findings provide the most comprehensive characterization of the CC2D1A interactome to date, elucidating novel, multifaceted, and dynamic cellular functions, providing potential implications for its role in neurodevelop-mental disorders.

molecular biology↗

Impact of maternal compensation on developmental phenotypes in a zebrafish model of severe congenital muscular dystrophy

Genetic compensation is a common phenomenon in zebrafish in response to genetic alterations. As such, differences between morphant and mutant zebrafish models of human diseases have led to significant difficulties in phenotypic interpretation and translatability. One form of compensation is the maternal deposit of mRNAs and proteins into the oocyte that supports developmental processes before zygotic genome activation. In this study, we generated a zebrafish model of severe congenital muscular dystrophy by targeting protein O-mannose N-Acetylglucosaminyltransferase 2 (pomgnt2), a maternally provided gene that maintains cell-extracellular matrix interactions through glycosylation. Zygotic knockouts (ZKOs) retain protein function in the first week post-fertilization and survive to adulthood, though they develop muscle disease later in life. In contrast, maternal-zygotic KOs (MZKOs) generated from ZKO females develop early-onset muscle disease, reduced motor function, neuronal axon guidance deficits, and retinal synapse disruptions, recapitulating features of the human presentation. While assessing transcriptional changes linked to disease progression, the availability of embryos obtained from different breeding strategies also allowed for direct comparison of ZKOs and MZKOs to define the impact of having a KO mother. We found that offspring from a ZKO mother, independently of genotype, show distinct expression patterns from animals obtained from heterozygous breeding. Some of these changes reflect an increased metabolic requirement, possibly stemming from maternal metabolic disruption. These findings will not only be applicable to other CMD models targeting maternally provided genes but also provide new insight into modeling disease using maternal-zygotic mutants.

genetics↗

Duplicated zebrafish (Danio rerio) inositol phosphatases inpp5ka and inpp5kb diverged in expression pattern and function

One hurdle in the development of zebrafish models of human disease is the presence of multiple zebrafish orthologs resulting from whole genome duplication in teleosts. Mutations in Inositol polyphosphate 5-phosphatase K (INPP5K) lead to a syndrome characterized by variable presentation of intellectual disability, brain abnormalities, cataracts, muscle disease, and short stature. INPP5K is a phosphatase acting at position 5 of phosphoinositides to control their homeostasis and is involved in insulin signaling, cytoskeletal regulation, and protein trafficking. Previously, our group and others have replicated the human phenotypes in zebrafish knockdown models by targeting both INPP5K orthologs inpp5ka and inpp5kb. Here, we show that inpp5ka is the more closely related orthologue to human INPP5K. While both inpp5ka and inpp5kb mRNA expression levels follow a similar trend in the developing head, eyes, and tail, inpp5ka is much more abundantly expressed in these tissues than inpp5kb. In situ hybridization revealed a similar trend, also showing unique localization of inpp5kb in the pineal gland indicating different transcriptional regulation. We also found that inpp5kb has lost its catalytic activity against its preferred substrate, PtdIns(4,5)P2. Since most human mutations are missense changes disrupting phosphatase activity, we propose that loss of inpp5ka alone can be targeted to recapitulate the human presentation. In addition, we show that the function of inpp5kb has diverged from inpp5ka and may play a novel role in the zebrafish.

developmental biology↗

A Data-Dependent Acquisition Ladder for Ultrasensitive (Neuro)Proteomics

Measurement of broad types of proteins from a small number of cells to single cells would help to better understand the nervous system but requires significant leaps in high-resolution mass spectrometry (HRMS) sensitivity. Microanalytical capillary electrophoresis electrospray ionization (CE-ESI) offers a path to ultrasensitive proteomics by integrating scalability with sensitivity. We report here a data acquisition strategy that expands the detectable and quantifiable proteome in trace amounts of digests using CE-ESI-HRMS. Data-dependent acquisition (DDA) was programmed to progressively exclude high-intensity peptide signals during repeated measurements. These nested experiments formed rungs of our "DDA ladder." The method was tested for replicates analyzing ~500 pg of protein digest from cultured hippocampal (primary) neurons (mouse), which estimates to the total amount of protein from a single neuron. Analysis of net amounts approximating to ~10 neurons identified 428 nonredundant proteins (415 quantified), an ~35% increase over traditional DDA. The identified proteins were enriched in neuronal marker genes and molecular pathways of neurobiological importance. The DDA ladder deepens the detectable proteome from trace amounts of proteins, expanding the analytical toolbox of neuroscience.

neuroscience↗

Cell-based analysis of CAD variants identifies individuals likely to benefit from uridine therapy

PurposePathogenic autosomal recessive variants in CAD, encoding the multienzymatic protein initiating pyrimidine de novo biosynthesis, cause a severe inborn metabolic disorder treatable with a dietary supplement of uridine. This condition is difficult to diagnose given the large size of CAD with over 1000 missense variants and the non-specific clinical presentation. We aimed to develop a reliable and discerning assay to assess the pathogenicity of CAD variants and to select affected individuals that might benefit from uridine therapy. MethodsUsing CRISPR/Cas9, we generated a human CAD-knockout cell line that requires uridine supplements for survival. Transient transfection of the knockout cells with recombinant CAD restores growth in absence of uridine. This system determines missense variants that inactivate CAD and do not rescue the growth phenotype. ResultsWe identified 25 individuals with biallelic variants in CAD and a phenotype consistent with a CAD deficit. We used the CAD-knockout complementation assay to test a total of 34 variants, identifying 16 as deleterious for CAD activity. Combination of these pathogenic variants confirmed 11 subjects with a CAD deficit, for whom we describe the clinical phenotype. ConclusionsWe designed a cell-based assay to test the pathogenicity of CAD variants, identifying 11 CAD deficient individuals, who could benefit from uridine therapy.

genetics↗

Male-specific CREB signaling in the hippocampus controls spatial memory deficits in a mouse model of autism and intellectual disability

BackgroundThe prevalence of neurodevelopmental disorders is biased towards males with male: female ratios of 2:1 in intellectual disability (ID) and 4:1 in autism spectrum disorder (ASD). However, the molecular mechanisms of such bias remain unknown. While characterizing a mouse model for loss of the signaling scaffold coiled-coil and C2 domain containing 1A (CC2D1A), which is mutated in ID and ASD, we identified biochemical and behavioral differences between males and females, and explored whether CC2D1A controls male-specific intracellular signaling.\n\nMethodsCC2D1A is known to regulate phosphodiesterase 4D (PDE4D). We tested for activation PDE4D and downstream signaling molecules such as CREB in the hippocampus of Cc2d1a-deficient mice. We then performed behavioral studies in females to analyze learning and memory, social interactions, anxiety and hyperactivity. Finally, we targeted PDE4D activation with a PDE4D inhibitor to define how changes in PDE4D and CREB activity affect behavior in males and females.\n\nResultsWe found that in Cc2d1a-deficient males PDE4D is hyperactive leading to a reduction in CREB signaling, but this molecular deficit is not present in females. Cc2d1a-deficient females only show impairment in novel object recognition, and no other cognitive and social deficits that have been found in males. Restoring PDE4D activity using an inhibitor rescues male-specific cognitive deficits, but has no effect on females.\n\nConclusionsOur findings show that CC2D1A regulates intracellular signaling in a male-specific manner in the hippocampus leading to male-specific behavioral deficits. We propose that male-specific signaling mechanisms are involved in establishing sex bias in neurodevelopmental disorders.

neuroscience↗